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Oligogalacturonides enhance cytokinin-induced vegetative shoot formation in tobacco explants, inhibit polyamine biosynthetic gene expression, and promote long-term remobilisation of cell calcium

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Abstract

Long-sized oligogalacturonides (OGs) are cell wall fragments that induce defence and developmental responses. The Ca2+-dependent “egg-box” conformation is required for their activity, and polyamines may prevent them from adopting this conformation. Although OGs are known to inhibit auxin-induced growth processes, their effect on cytokinin-induced ones requires investigation. In the present work OGs were shown to promote cytokinin (benzyladenine, BA)-induced vegetative shoot formation from tobacco leaf explants, independent of the presence of CaCl2 in the medium and of auxin (indoleacetic acid, IAA) supply. The effect of polyamines, putrescine (PU) and spermidine (SD) supplied with/without their biosynthetic inhibitors (DFMO, CHA) was also investigated, and showed that spermidine enhanced adventitious vegetative shoot formation, but only on medium containing Ca2+ and IAA. Treatments with inhibitors blocked this promotive effect. OGs did not alter free polyamine concentrations, but caused a moderate increase of conjugated ones, and exhibited an early inhibitory effect on polyamine biosynthetic gene expression. OGs, but not SD, caused long-term changes in calcium-associated epifluorescent signals in the cell walls, and, later, inside the cells of specific tissues. Electron microscopy analysis (ESI system) demonstrated that calcium accumulated in the cell walls and vacuoles of OG-cultured explants. The relationship between OGs, cytokinin, calcium, and polyamines in adventitious vegetative shoot formation is discussed.

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Abbreviations

ADC:

Arginine decarboxylase

BA:

N6-benzyladenine

AU:

Arbitrary unit

CHA:

Cyclohexylamine

CTC:

Chlorotetracycline

CW:

Cell wall

CWC:

Cell wall corner

DFMO:

dl-α-difluoromethylornithine

DP:

Degree of polymerisation

EDTA:

Ethylenediaminetetraacetic acid

EGTA:

Ethylene glycol-bis-(β aminoethyl ether)- N,N,N′N′-tetraacetic acid

ESI:

Electron spectroscopy images

FAA:

Ethanol:glacial acetic acid:formalin

IAA:

Indoleacetic acid

ODC:

Ornithine decarboxylase

OG(s):

Oligogalacturonide(s)

PA(s):

Polyamine(s)

PU:

Putrescine

SAMDC:

S-adenosylmethionine decarboxylase

SD:

Spermidine

SPD synt:

Spermidine synthase

VSF:

Vegetative shoot-forming

SM:

Spermine

V:

Vacuole

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Acknowledgments

The cDNA probes for ADC, ODC, and SAMDC were kindly supplied by Anthony J. Michael (Institute of Food Research, Norwich, UK). The authors are grateful to Antonella Canini (Dipartimento di Biologia, Università di Roma “Tor Vergata”, Italy) for the help in the electron microscopy, and to Daniela Bellincampi and Giulia De Lorenzo (Dipartimento di Biologia Vegetale, Università La Sapienza, Rome, Italy) and Roberto Moscatiello (Dipartimento di Biologia, Università di Padova, Italy) for kindly providing the OGs. They also thank Giulia Tronelli for technical support. Funding by Progetto d’Ateneo, Università La Sapienza, Rome (to MMA) and by the RFO (ex-60%), University of Bologna (to SB) is acknowledged.

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Authors and Affiliations

  1. Dipartimento di Biologia Vegetale, Università di Roma “La Sapienza”, Rome, Italy

    Giuseppina Falasca, Francesca Capitani, Federica Della Rovere, Daniela Zaghi & Maria Maddalena Altamura

  2. Dipartimento di Biologia Evoluzionistica Sperimentale, Università di Bologna, Bologna, Italy

    Cinzia Franchin & Stefania Biondi

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  1. Giuseppina Falasca
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  2. Francesca Capitani
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  3. Federica Della Rovere
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  4. Daniela Zaghi
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  5. Cinzia Franchin
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  6. Stefania Biondi
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  7. Maria Maddalena Altamura
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Correspondence to Maria Maddalena Altamura.

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Falasca, G., Capitani, F., Della Rovere, F. et al. Oligogalacturonides enhance cytokinin-induced vegetative shoot formation in tobacco explants, inhibit polyamine biosynthetic gene expression, and promote long-term remobilisation of cell calcium. Planta 227, 835–852 (2008). https://doi.org/10.1007/s00425-007-0660-6

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